Changes in soil quality after converting Pinus to Eucalyptus plantations in southern China

Vegetation plays a key role in maintaining soil quality, but long-term changes in soil quality due to plant species change and successive planting are rarely reported. Using the space-for-time substitution method, adjacent plantations of Pinus and first, second, third and fourth generations of Eucalyptus in Guangxi, China were used to study changes in soil quality caused by converting Pinus to Eucalyptus and successive Eucalyptus planting. Soil chemical and biological properties were measured and a soil quality index was calculated using principal component analysis. Soil organic carbon, total nitrogen, alkaline hydrolytic nitrogen, microbial biomass carbon, microbial biomass nitrogen, cellobiosidase, phenol oxidase, peroxidase and acid phosphatase activities were significantly lower in the first and second generations of Eucalyptus plantations compared with Pinus plantation, but they were significantly higher in the third and fourth generations than in the first and second generations and significantly lower than in Pinus plantation. Soil total and available potassium were significantly lower in Eucalyptus plantations (1.8–2.5 g kg and 26–66 mg kg) compared to the Pinus plantation (14.3 g kg and 92 mg kg), but total phosphorus was significantly higher in Eucalyptus plantations (0.9– 1.1 g kg) compared to the Pinus plantation (0.4 g kg). As an integrated indicator, soil quality index was highest in the Pinus plantation (0.92) and lowest in the first and second generations of Eucalyptus plantations (0.24 and 0.13). Soil quality index in the third and fourth generations (0.36 and 0.38) was between that in Pinus plantation and in first and second generations of Eucalyptus plantations. Changing tree species, reclamation and fertilization may have contributed to the change observed in soil quality during conversion of Pinus to Eucalyptus and successive Eucalyptus planting. Litter retention, keeping understorey coverage, and reducing soil disturbance during logging and subsequent establishment of the next rotation should be considered to help improving soil quality.


Introduction
Vegetation plays a key role in soil development due to its influence on nutrient cycling, hydrological processes and soil erosion (de la Paix et al., 2013;Zhao et al., 2013).Degradation of soil quality is a serious problem (Miao et al., 2012;Zhao et al., 2013).Eucalyptus is an important tree species for afforestation in tropical and subtropical regions and has been introduced to many countries around the world.In southern China, millions of hectares of degraded land, cropland and natural secondary forest have been converted into Eucalyptus plantations and successive planting has been undertaken (Wen et al., 2009).However, due to nutrient limitations in many areas (LeBauer and Treseder, 2008) and a high demand for nutrients by Eucalyptus (Laclau et al., 2010), this kind of land use change may exhaust soil nutrients and decrease soil quality (Yu et al., 2000b).Inappropriate plantation management also accelerates the decline in soil quality (Yu et al., 2009).There is an urgent need to assess the effects that Eucalyptus planting has on soil quality since it plays a key role in sustaining forest productivity.
Soil quality includes soil physical, chemical and biological properties, as well as soil processes and their interactions (Andrews and Carroll, 2001).Many studies have focused on soil physic-chemical properties (Garay et al., 2004;Muñoz-Rojas et al., 2012;Parras-Alcántara et al., 2013), microbial communities (Wu et al., 2012) or enzyme activities (Wang et al., 2008), which only reflect some aspects of soil quality.A soil quality index (SQI) was proposed for quantifying the combined biological, chemical and physical response of soil to land use and soil/crop management practices (Andrews and Carroll, 2001;Andrews et al., 2002).It provides an intelligible and more holistic measurement of soil quality and, in recent years, the SQI has been used to assess the impacts of land use change, forest and cropland management and ecological restoration (Navas et al., 2011;Morugán-Coronado et al., 2013;Tesfahunegn, 2013).Methods used to calculate SQI include expert opinion and principal component analysis (PCA) (Andrews et al., 2002), with the latter more widely used in recent studies (Navas et al., 2011).
The ecological consequences of Eucalyptus planting are important and have been studied in depth.For example, it was reported that soil organic carbon, nitrogen, microbial biomass and the metabolic quotient were significantly lower in Eucalyptus plantations compared to natural and regenerated forests or pastures (Behera and Sahani, 2003;Sicardi et al., 2004;Araújo et al., 2010;Chen et al., 2013).It was also found that the conversion of native savanna or sugarcane fields to Eucalyptus plantations did not cause impacts on soil organic carbon, microbial biomass carbon or nitrogen contents (Binkley et al., 2004).Fialho and Zinn (2014) compiled paired-plot studies on how soil organic carbon stocks under native vegetation change after planting fast-growth Eucalyptus species in Brazil and found that Eucalyptus plantations on average had no net effect on soil organic carbon stocks.The results of these different studies were not consistent and the effect of successive Eucalyptus planting has rarely been reported.
Here we accessed the effects of converting Pinus to Eucalyptus and subsequent successive Eucalyptus planting on soil quality by examining adjacent plantations of local Pinus massoniana Lamb.(Pinus) and first, second, third and fourth generations of Eucalyptus urophylla x grandis (Eucalyptus).The changes in soil quality were investigated by measuring the soil chemical and biological properties and by calculating a SQI using the PCA method for each plantation.Exhaustion of soil nutrients was the main problem considered in the studied Eucalyptus plantation; soil physical attributes were not considered in this study.The study aimed to test the effect on soil bio-chemical quality after (1) converting Pinus to Eucalyptus plantations and (2) successive Eucalyptus planting with rotation time of 5 years in southern China.

Study area
This study was conducted at Fusui, Guangxi, China (22 • 14 -22 • 21 N, 107 • 47 -107 • 56 E; Fig. 1).Elevation of study sites was between 140 and 250 m above sea level.The dominant aspect of slopes was southeast, with slope below 15 • .The region has a typical subtropical monsoon climate with mean annual temperature of 21.2-22.3• C. Annual rainfall is 1100-1300 mm, concentrated during June-August.Soils in the region are mainly lateritic red earth with a profile depth of more than 80 cm.Soil pH ranged from 4 to 5 (Chen et al., 2013).
Before the 1980s, this area was dominated by Pinus massoniana Lamb.(Pinus), with 30-year rotation (clearing and new planting), used for fire wood, timber and oil production.In the 1980s, fast-growing Eucalyptus urophylla x grandis (Eucalyptus) with a 5-year rotation period began to replace Pinus.The first generation of Eucalyptus was planted with a density of about 1400 trees ha −1 after clear-cutting, fire clearance and full reclamation (plowed to 50 cm depth).The second generation of Eucalyptus was regenerated by sprouts.The third generation of Eucalyptus was planted with seedlings after strip reclamation (50 cm depth).Finally, the fourth generation was regenerated by sprouts again.Leaves, branch and bark litter were kept in the plantation during the plant growth period.However, at harvest time, most branch litter was removed and burned before the next rotation, and soil erosion happened easily due to the lack of soil protection during the crop transition periods.Before Eucalyptus planting, base fertilizer (500 g seedling −1 , N : P : K = 10 : 15 : 5) was added into a 20 cm depth soil hole under each new Eucalyptus tree and covered with soil.Then, 6, 12 and 24 months after planting, 250, 500 and 500 g, respectively, of fertilizer (N : P : K = 15 : 10 : 8) per tree was separately added in soil holes that were 30 cm away from each tree.Herbicide (glyphosate) was applied once a year during the first 3 years after Eucalyptus planting and consequently the coverage of understory plants was less than 50 %.However, the understory coverage increased gradually during the fourth and fifth years after Eucalyptus planting.During sampling time, tree, shrub and grass cover in the Pinus plantation was about 60, 25 and 70 %, respectively.Tree, shrub and grass cover in the Eucalyptus plantations was similar, about 40, 10 and 45 %, respectively.The litter layer was about 3 cm in the Pinus plantation and 1 cm deep in the Eucalyptus plantations.

Experimental design and sampling
The adjacent plantations of local Pinus and first, second, third and fourth generations of Eucalyptus at the Dongmen Forestry Farm were selected (Fig. 1) to represent Pinus planting and first, second, third and fourth generations of successive Eucalyptus planting.Three 20 m × 20 m plots were randomly selected and marked out at each plantation site, with an average distance of 20 m between plots.During soil sampling, the ages of Pinus and Eucalyptus was 20 and 3 years, respectively.
In October 2010, soil from the top 0-10 cm layer was collected from the study sites.Ten soil cores were collected at randomly selected points at each plot using a 3.6 cm diameter soil auger and mixed together as a composite sample.Three composite samples were collected at each point.Stones and roots were removed from the soil samples by hand and soil samples were sieved through 2 mm sieves.Soil samples were stored at 4 • C for soil microbial biomass and enzyme activity analyses, or air dried for chemical analyses.

Soil chemical and biological analyses
Soil water content was determined gravimetrically after oven-drying at 105 • C for 24 h in order to correct sample weights in biochemical property measurements.Soil pH was measured in deionized water (1 : 2.5 w/v) using a Delta 320 pH-meter (Mettler-Toledo Instruments (Shanghai) Co., Ltd.).Soil organic carbon (SOC) was measured using the Walkley and Black wet oxidation method as outlined in Bao (2000).Soil total nitrogen (TN) was determined by combustion in a Vario EL III Elemental Analyser (Elementar Analysensysteme GmbH, Germany).Soil alkaline hydrolytic nitrogen (AN) was measured according to Bao (2000).For the assessment of AN, 1 g of air-dried soil was incubated in 5 mL sodium hydroxide solution (1.2 M) in the outside ring of an airtight Conway diffusion cell; 3 mL boric acid (0.3 M) were added to the inner well at 40 • C for 24 h.With methyl red-bromocresol green as indicator, 0.01 M hydrochloric acid was used to titrate ammonia absorbed in the boric acid.For total phosphorus (TP) and total potassium (TK), air-dried soil samples were digested using 18.4 M sulfuric acid (1 : 10 w/v) and 12.7 M perchloric acid at 275 • C for 6 h, TP and TK were measured using a Prodigy High Dispersion ICP-OES (Teledyne Technologies Incorporated, USA).Available phosphorus (AP) was measured after extraction with 0.05 N sulfuric and 0.025 N hydrochloric acids acetate solution (1 : 10 w/v), shaken for 30 min (Bao, 2000).AP and AK were measured using the Prodigy High Dispersion ICP-OES.Soil microbial biomass carbon and nitrogen (MBC and MBN, respectively) were estimated using the chloroform fumigation extraction method (Vance et al., 1987).Soil βglucosidase (BG), phenol oxidase (PO), peroxidase (POD) and acid phosphatase (ACP) activities were measured according to Waldrop et al. (2000).Soil protease (PRO) activity was estimated according to Ladd and Butler (1972).Soil urease (URE) activity was assessed according to Kandeler and Gerber (1988).Soil cellobiosidase (CBH) activity was measured using the fluorimetric method according to Saiya-Cork et al. (2002).

Calculation of the soil quality index
The SQI was calculated according to Andrews and Carroll (2001).Three steps were involved in the elaboration of this quality index: (i) definition of a minimum data set (MDS), (ii) assignment of a score to each indicator by linear scoring functions and (iii) data integration into an index.
Three steps were used to identify the MDS in our study.( 1) Data screening: one-way analysis of variance was performed for soil chemical and biological properties; only variables with significant differences between treatments (p < 0.05) were chosen for the next step.(2) Selection of representative variables: PCA was performed on the variables chosen from step (1); only principal components (PCs) that explained at least 5 % of the variation in the data up to 85 % of the cumulative variation were examined, within each PC, only weighted factors with absolute values within 10 % of the highest weight were retained for the MDS.(3) Redundancy reduction: multivariate correlation coefficients were used to determine the strength of the relationships among variables.Highly correlated variables (correlation coefficient > 0.70) were considered redundant and candidates for elimination from the data set.In order to choose variables within wellcorrelated groups, we summed the absolute values of the correlation coefficients for these variables and assumed that the variable with the highest correlation sum best represented the group.The choice among well-correlated variables was also based on the published references and expert opinion about the soils and sites (Xu, 2000;Wang et al., 2008;Yu et al., 2009).Any uncorrelated, highly weighted variables were considered important and retained in the MDS.
Linear scoring was used in our study.Indicators were ranked in ascending or descending order depending on whether a higher value was considered "good" or "bad" in terms of soil function.In our study, all variables were "more is better".The linear scoring function used for converting measured values to scored values is as follows (Zheng et al., 2005): where S ij is the score of soil variable i of sample j , V ij is the observed variable value of sample j , V i max is the highest value of variable i, and V i min is the lowest value of variable i.
The scores of the indicators (Table 1) were integrated into a SQI according to Andrews et al. (2002) as follows: where S i is the score assigned to indicator i, and n is the number of indicators included in the MDS.

Statistical analyses
One-way variance analyses were used to test the significant differences in soil chemical and biological properties and SQIs among these treatments.Normality of the data was tested using the Kolmogorov-Smirnov test and the soil indicators obeyed standard normal distribution.Tukey's test was used for multiple comparison analysis.All statistical analyses were performed using SPSS 10.0 (SPSS Inc., Chicago, IL, USA) and SigmaPlot for Windows version 11.0 (Systa Software Inc.).The three plots established per site do not constitute true replicates, because they are located within the same area of the five plantations (Pinus, first, second, third and fourth generations Eucalyptus plantations).However, these plantation stands occur in similar topographic conditions and soil parent material, and were similar in planting history (Pinus plantation before the 1980s), which allowed us to consider them as different treatments.

Soil chemical properties
SOC, TN and AN ranges at our study sites were 10.8-26.9g kg −1 , 0.9-1.6 g kg −1 and 41.4-60.3mg kg −1 , respectively.They were high in the Pinus plantation, low in the first and second generations of Eucalyptus plantations, and moderate in the third and fourth generations (Fig. 2a-c).SOC and TN in the fourth generation of Eucalyptus plantations were significantly lower than in the Pinus plantation, but significantly higher than in the second generation of Eucalyptus plantations.Soil AN in the fourth generation of Eucalyptus was significantly higher than in the second generation, but not different from that in the Pinus plantation.Soil TP content was significantly lower in the Pinus plantation (0.41 g kg −1 ) than in the Eucalyptus plantations (0.90-1.07 g kg −1 ).In the Eucalyptus plantations, soil TP content was significantly lower in the second generation than in the third and fourth generations (Fig. 2d).Soil AP content was 2.98 mg kg −1 in the Pinus plantation, which is lower than 5.03 and 5.14 mg kg −1 in the first and second generations of Eucalyptus plantations, respectively, a little higher than 2.56 and 2.93 mg kg −1 in the third and fourth generations, respectively (Fig. 2e).
Soil TK and AK ranged from 1.8 to 6.3 g kg −1 and from 24 to 92 mg kg −1 , respectively.TK content was significantly lower in the Eucalyptus plantations than in the Pinus plantation, without significant differences between Eucalyptus generations (Fig. 2f).AK content was significantly higher in the Pinus plantation compared with in Eucalyptus plantations (Fig. 2g).

Soil microbial biomass carbon and nitrogen
Soil MBC and MBN contents ranged from 278 to 673 mg kg −1 and from 7 to 35 mg kg −1 , respectively.Soil MBC content was significantly lower in the first and second generation of Eucalyptus plantations than in the third and fourth generations (Fig. 3a).Soil MBN content was significantly lower in the second generation (Fig. 3b).The MBC / MBN ratio was significantly higher in the second generation Eucalyptus plantation than in other plantations (Fig. 3c).

Soil enzyme activities
BG activity was significantly higher in the Pinus plantation compared with in Eucalyptus plantations (Fig. 4a).Soil CBH, PO, POD, PRO and ACP activities were highest in the Pinus plantation, lowest in the first or second generations of Eucalyptus plantations and between the middle in the third or fourth generations of Eucalyptus plantations (Fig. 4b-f).Soil URE activity was significantly higher in the Pinus plantation than in the Eucalyptus plantations, with no significant differences among Eucalyptus plantations (Fig. 4g).

Changes in soil quality index
SQI was highest in the Pinus plantation (0.92) and lowest in the second generation of the Eucalyptus plantations (0.13).In the third and fourth Eucalyptus generations, SQI was significantly higher than in the second Eucalyptus generation (0.36 and 0.38, respectively, compared to 0.13), but still lower than in the Pinus plantation (0.92, Fig. 5).

Decrease in soil quality in the first and second generations of Eucalyptus planting
Our study found that SOC, TN, AN, TK, AK, MBC, MBN and enzyme activities significantly decreased in the first and second generation Eucalyptus plantations after converting Pinus to Eucalyptus (Figs. 2-4).This is consistent with many studies which reported that SOC, TN, MBC, carbon metabolic activity and metabolic quotient were significantly lower in Eucalyptus plantations than in natural and regenerated forest or pastures (Behera and Sahani, 2003; Sicardi  et al., 2004;Chen et al., 2013).However, in our study, soil TP was significantly higher in Eucalyptus plantation, which might be caused by fertilization in Eucalyptus plantations and the low mobility of phosphorus.The decreased soil quality in the first and second generations of Eucalyptus plantations after converting Pinus to Eucalyptus plantation may have been caused by tree species change, full reclamation, herbicide application, clear-cutting and short rotation.
Eucalyptus has a fast growth rate and a strong nutrient absorption capacity, which means that they absorb soil nutrients and store them in the biomass efficiently (Laclau et al., 2005), resulting in lower nutrient contents in the soil (Fig. 2).Tesfaye et al. ( 2014) evaluated seven tree species for fuelwood and soil restoration and found that Eucalyptus presented the highest growth rates and biomass, but depleted soil nitrogen.The depletion of nitrogen in soils under Eucalyptus plantations was also found by Wen et al. (2009).The lower soil nutrient contents in the second generation Eucalyptus plantation may lead to lower soil microbial biomass and enzyme activities and a higher MBC / MBN ratio (Figs. 3,4).
Full reclamation normally impacts the soil structure, exposes more aggregates and accelerates organic matter de- composition (Zinn et al., 2002), which would lead to lower soil organic matter contents in the Eucalyptus plantations.Understorey vegetation may provide a better microcosm for microorganisms and alleviate rainfall-induced erosion and nutrient leaching (Yu et al., 2000a).In our study, herbaceous vegetation was treated with herbicide during the first 3 years of the Eucalyptus planting exposing the uncovered soils to erosion.
At harvest, clear-cutting totally destroyed plant coverage and the subsequent fire clearance burned all the residues and the litter layer, which resulted in bare ground prior to Eucalyptus planting.Soil erosion and nutrient leaching can occur during heavy rainfall if there is no protection from plant and litter layers (Yu et al., 2000a).Fire also removes significant amounts of organic matter (Certini, 2005) and nutrients are lost through volatilization (Fisher and Binkley, 2000).Soil microbial biomass decreases during fire because of increased decay and death of heat-sensitive microbes or through alterations of soil physic-chemical properties (De Marco et al., 2005).These could have been the causes for the bio-chemical depletion observed in soils that underwent Pinus to Eucalyptus conversion.
Eucalyptus cultivation rotations are very short (only 5 years) compared to Pinus (30 years), which means that there is frequent biomass loss in Eucalyptus plantations.Furthermore, short rotations have an impact on the nutrient absorption patterns and the soil nutrient returns.During the early stages of plant life, nutrient absorption is high and litter production is small, but as the plant gets older nutrient absorption decreases and litter production increases (Xu, 2000).The 5-year rotation of Eucalyptus plantations and frequent cutting led to severe soil nutrient loss.

Increase in soil quality in the third and fourth generations of Eucalyptus planting
Our results showed that after the sudden decline following converting Pinus to Eucalyptus, SOC, TN, MBC, CBH, PO, POD and ACP activities recovered in the third and fourth generations, albeit lower than that in the native Pinus plantation (Figs.2-4).This is inconsistent with Yu et al. (2000b), who recorded that soil physical and chemical properties decreased during successive Eucalyptus planting.However, Lima et al. (2006) recorded an increasing soil organic matter trend as the plantation aged after Eucalyptus afforestation of degraded pastures.The inconsistency between these studies might be caused by different climate, soil properties, Eucalyptus species and management practices amongst the study sites.The recovery of soil quality in the third and fourth generation Eucalyptus plantations may be attributed to reduced soil disturbance and fertilizer application.Soil disturbance caused by strip reclamation in the third generation Eucalyptus plantation was much smaller than that due to full reclamation during the conversion from Pinus to Eucalyptus, which may have led to a reduction in soil organic matter decomposition, soil erosion and nutrient leaching.The decreased soil erosion risk, nutrient leaching and organic matter decomposition rate helped in improving soil organic matter accumulation and nutrient levels (Yu et al., 2000a).
Fertilization could increase plant growth and litter input (Madeira et al., 1995), so improving soil quality.If soil nutrient inputs through fertilization and litter fall equal the output caused by erosion, plant absorption and leaching, then soil quality would reach a steady status (Xu, 2000).Our results suggest a recovery in soil quality after the third and fourth generations of Eucalyptus planting (Fig. 5).To better understand the impacts of successive Eucalyptus planting on soil quality, evaluation of more generations of Eucalyptus plantations is needed.

Conclusions
Findings from our study suggest that soil quality decreased significantly in the first and second generation Eucalyptus plantations after converting Pinus to Eucalyptus plantations, partially recovering in the following third and fourth generations.Changes in tree species, reclamation, herbicide application and long-term fertilization might have contributed to the changes observed in the soil quality during successive Eucalyptus planting.Our results emphasize the importance of long-term soil quality monitoring.Improving management practices, such as maintenance of litter and herbaceous cover and reduction of soil disturbance during logging and subsequent establishment of the next planting rotation, should be considered to maintain soil quality.
Author contributions.H. Zheng and Z. Y. Ouyang designed the experiment and K. Zhang, F. L. Chen, and Y. Wang carried it out.Y. F. Wu, J. Lan, M. Fu and X. W. Xiang helped collecting soil samples and gave suggestion about the experiment.K. Zhang and H. Zheng prepared the paper.

Figure 1 .
Figure 1.Study site and pictures of the Pinus and the successive Eucalyptus plantations.MP, G1, G2, G3 and G4 refer to the Pinus plantation and the first, second, third and fourth generation Eucalyptus plantations, respectively.

Figure 2 .
Figure 2. Soil chemical properties in the Pinus and the successive Eucalyptus plantations.MP, G1, G2, G3 and G4 refer to the Pinus plantation and the first, second, third and fourth generation Eucalyptus plantations, respectively.SOC, soil organic carbon; TN, total nitrogen; TP, total phosphorus; TK, total potassium; AN, alkaline hydrolytic nitrogen; AP, available phosphorus and AK, available potassium.Soil chemical properties with the same letter are not significantly different at p < 0.05.

Figure 3 .
Figure 3. Soil microbial biomass carbon and nitrogen in the Pinus and the successive Eucalyptus plantations.MP, G1, G2, G3 and G4 refer to the Pinus plantation and the first, second, third and fourth generation Eucalyptus plantations, respectively.MBC, microbial biomass carbon and MBN, microbial biomass nitrogen.Microbial indicators with the same letter are not significantly different at p < 0.05.

Figure 4 .
Figure 4. Soil enzyme activities in the Pinus and the successive Eucalyptus plantations.MP, G1, G2, G3 and G4 refer to the Pinus plantation and the first, second, third and fourth generation Eucalyptus plantations, respectively.BG, β-glucosidase; CBH, cellobiosidase; PO, phenoloxidase; POD, peroxidase; PRO, protease; URE, urease and ACP, acid phosphatase.Enzyme activities with the same letter are not significantly different at p < 0.05.

Figure 5 .
Figure 5. Soil quality index in the Pinus and the successive Eucalyptus plantations.MP, G1, G2, G3 and G4 refer to the Pinus plantation and the first, second, third and fourth generation Eucalyptus plantations, respectively.SQI, soil quality index.SQIs with the same letter are not significantly different at p < 0.05.

Table 1 .
Soil quality indicator scores (mean ± standard error) for soil samples taken from the Pinus and Eucalyptus plantations.